A phylogenetic hypothesis for the origin of hiccough

Abstract

The occurrence of hiccoughs (hiccups) is very widespread and yet their neuronal origin and physiological significance are still unresolved. Several hypotheses have been proposed. Here we consider a phylogenetic perspective, starting from the concept that the ventilatory central pattern generator of lower vertebrates provides the base upon which central pattern generators of higher vertebrates develop. Hiccoughs are characterized by glottal closure during inspiration and by early development in relation to lung ventilation. They are inhibited when the concentration of inhaled CO(2) is increased and they can be abolished by the drug baclofen (an agonist of the GABA(B) receptor). These properties are shared by ventilatory motor patterns of lower vertebrates, leading to the hypothesis that hiccough is the expression of archaic motor patterns and particularly the motor pattern of gill ventilation in bimodal breathers such as most frogs. A circuit that can generate hiccoughs may persist in mammals because it has permitted the development of pattern generators for other useful functions of the pharynx and chest wall muscles, such as suckling or eupneic breathing.

Dynamic Changes in Glottal Resistance during Exposure to Severe Hypoxia in Neonatal Rats In Situ

“…To our knowledge, the only respiratoryrelated activity correlating with inspiratory glottal closure is the hiccup (34). It is interesting that the hiccup is apparently one of the first respiratory-related activities reported for the mammalian fetus.…”

“…According to the theory that evolution is reflected by the gestational stages of the embryo, this might suggest that the hiccup has an old origin. Indeed, in a recent article by Strauss et al (34) it was reviewed that the hiccup potentially reflects the most archaic form of breathing-this being gill ventilation, which is characterized by synchronous activation of inspiratory muscles during glottal closure. Therefore, a progressing failure of respiratory network function during hypoxia may potentially reveal ancient forms of breathing that were not designed for air breathing.…”

Hiccups due to Central Nervous System Disease: Analysis of 71 Inpatients

“…1 Hiccups of CNS origin usually arise from direct medullary damage. However, occasional reports of persistent hiccups attributed to cerebral lesions, the four cerebral cases in the present study, and an 11% incidence of hiccups following pallidotomy 3,4 all suggest that descending medullary influences may evoke hiccup on occasion.…”

“…In bypassing the lungs to direct water to their gills, our tadpole ancestors may have bequeathed hiccups to man 1 . Central nervous system (CNS) lesions presumably disinhibit this primitive synkinesis in which the diaphragm is joined in a coordinated movement by intercostal and accessory respiratory muscles, as well as pharyngeal (rarely mentioned but easily observed) and laryngeal muscles.…”

Vestiges of the natural history of development: historical holdovers reveal the dynamic interaction between ontogeny and phylogeny

“…These range from biochemical reactions or physiological properties, such as the mammalian dive reflex (present in humans but in much-reduced form relative to other mammals; Elsner and Gooden 1983), to biogeographic distributions of relict taxa, indicators of formerly larger populations. Straus et al (2003) hypothesized that hiccups are a vestigial motor reflex pattern (of glottal closure during inhalation, so that the vocal folds slam shut) left over from early tetrapod vertebrates, specifically the tadpole larvae of amphibians. Tadpoles undergo a ventilatory transformation from external filamentous gills to pulmonary respiration, with a consequent need to close lungs to avoid ingesting water, which is diverted to gills instead (Shubin 2008).…”